Abstract
Root hairs (RHs) are single-celled elongated epidermal cells and play a vital role in nutrient absorption, particularly for immobile minerals like phosphorus (P). As an adaptive response to P deficiency, an increase in RH length enhances root-soil contact and absorptive area for P absorption. Genetic variations have been reported for RH length and its response to P deficiency in plants. However, only a few association studies have been conducted to identify genes and genetic loci associated with RH length. Here, we screened desi chickpea accessions for RH length and its plasticity under P deficiency. Further, the genome-wide association study (GWAS) was conducted to identify the genetic loci associated with RH length in P deficient and sufficient conditions. Although high variability was observed in terms of RH length in diverse genotypes, majority of the accessions showed typical response of increase in RH length in low P. Genome-wide association mapping identified many SNPs with significant associations with RH length in P-sufficient and P-deficient conditions. A few candidate genes for RH length in P deficient (SIZ1-like and HAD superfamily protein) and sufficient (RSL2-like and SMAP1-like) conditions were identified which have known roles in RH development and P deficiency response or both. Highly associated loci and candidate genes identified in this study would be useful for genomic-assisted breeding to develop P-efficient chickpea.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anon (2018) 4th Advance estimate of Production of Foodgrains for 2017– 18. Directorate of Economics & Statistics, Department of Agriculture, Cooperation and Farmers’ Welfare, Ministry of Agriculture and Farmers’ Welfare, Government of India. https://eands.dacnet.nic.in/Advance_Estimate/4th_Adv_Estimates2017-18_Eng.pdf. Accessed 17 Oct 2018
Balcerowicz D, Schoenaers S, Vissenberg K (2015) Cell fate determination and the switch from diffuse growth to planar polarity in Arabidopsis root epidermal cells. Front Plant Sci 6:1163. https://doi.org/10.3389/fpls.2015.01163
Barber SA (1962) A diffusion and mass-flow concept of soil nutrient availability. Soil Sci 93:39–49
Basu U, Upadhyaya HD, Srivastava R, Daware A, Malik N, Sharma A, Bajaj D, Narnoliya L, Thakro V, Kujur A, Tripathi S, Bharadwaj C, Hegde VS, Pandey AK, Singh AK, Tyagi AK, Parida SK (2019) Abc transporter-mediated transport of glutathione conjugates enhances seed yield and quality in chickpea. Plant Physiol 180:253–275. https://doi.org/10.1104/pp.18.00934
Bates T, Lynch J (1996) Stimulation of root hair elongation in Arabidopsis thaiiana by low phosphorus availability. Plant Cell Environ 19:529–538
Bhosale R, Giri J, Pandey BK, Giehl RFH, Hartmann A, Traini R, Truskina J, Leftley N, Hanlon M, Swarup K, Rashed A, Voß U, Alonso J, Stepanova A, Yun J, Ljung K, Brown KM, Lynch JP, Dolan L, Vernoux T, Bishopp A, Wells D, von Wirén N, Bennett MJ, Swarup R (2018) A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate. Nat Commun 9:1409. https://doi.org/10.1038/s41467-018-03851-3
Bobrownyzky J (2016) Production of branched root hairs under progressive drought stress in Arabidopsis thaliana. Cytol Genet 50:324–329. https://doi.org/10.3103/S0095452716050030
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Brown LK, George TS, Thompson JA, Wright G, Lyon J, Dupuy L, Hubbard SF, White PJ (2012) What are the implications of variation in root hair length on tolerance to phosphorus deficiency in combination with water stress in barley (Hordeum vulgare)? Ann Bot 110:319–328. https://doi.org/10.1093/aob/mcs085
Brown LK, George TS, Dupuy LX, White PJ (2013) A conceptual model of root hair ideotypes for future agricultural environments: What combination of traits should be targeted to cope with limited P availability? Ann Bot 112:317–330. https://doi.org/10.1093/aob/mcs231
Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, Pérez-Pérez J, Solano R, Leyva A, Paz-Ares J (2010) A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in arabidopsis. PLoS Genet 6:e1001102. https://doi.org/10.1371/journal.pgen.1001102
Cordell D, White S (2011) Peak phosphorus: Clarifying the key issues of a vigorous debate about long-term phosphorus security. Sustainability 3:2027–2049. https://doi.org/10.3390/su3102027
El-Gebali S, Mistry J, Bateman A et al (2019) The Pfam protein families database in 2019. Nucleic Acids Res 47:D427–D432. https://doi.org/10.1093/nar/gky995
FAO (2015) World fertilizer trends and outlook to 2018, Food and Agriculture Organization of the United Nations, Rome, Italy
FAOSTAT Statistical Database (2017) Food and Agriculture Organization of the United Nations, Rome, Italy. http://www.fao.org/faostat/en/#home. Accessed 7 Jan 2020
Gahoonia TS, Nielsen NE (2004) Barley genotypes with long root hairs sustain high grain yields in low-P field. Plant Soil 262:55–62
Gahoonia TS, Care D, Nielsen NE (1997) Root hairs and phosphorus acquisition of wheat and barley cultivars. Plant Soil 191:181–188
Gahoonia TS, Ali R, Malhotra RS (2007) Variation in root morphological and physiological traits and nutrient uptake of chickpea genotypes. J Plant Nutr 30:829–841. https://doi.org/10.1080/15226510701373213
Giri J, Bhosale R, Huang G, Pandey BK, Parker H, Zappala S, Yang J, Dievart A, Bureau C, Ljung K, Price A, Rose T, Larrieu A, Mairhofer S, Sturrock CJ, White P, Dupuy L, Hawkesford M, Perin C, Liang W, Peret B, Hodgman CT, Lynch J, Wissuwa M, Zhang D, Pridmore T, Mooney SJ, Guiderdoni E, Swarup R, Bennett MJ (2018) Rice auxin influx carrier OsAUX1 facilitates root hair elongation in response to low external phosphate. Nat Commun 9:1408. https://doi.org/10.1038/s41467-018-03850-4
Haling RE, Brown LK, Bengough AG, Young IM, Hallett PD, White PJ, George TS (2013) Root hairs improve root penetration, root-soil contact, and phosphorus acquisition in soils of different strength. J Exp Bot 64:3711–3721. https://doi.org/10.1093/jxb/ert200
Hasan BR (1996) Phosphorus Status of Soils in India. Crops 10:4–5
Ho J, Tumkaya T, Aryal S, Choi H, Claridge-Chang A (2019) Moving beyond P values: data analysis with estimation graphics. Nat Methods 16:565–566. https://doi.org/10.1038/s41592-019-0470-3
Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. Circ - Calif Agric Exp Stn 347:2nd edit
Holz M, Zarebanadkouki M, Kuzyakov Y, Pausch J, Carminati A (2018) Root hairs increase rhizosphere extension and carbon input to soil. Ann Bot 121:61–69. https://doi.org/10.1093/aob/mcx127
Huang G, Liang W, Sturrock CJ, Pandey BK, Giri J, Mairhofer S, Wang D, Muller L, Tan H, York LM, Yang J, Song Y, Kim YJ, Qiao Y, Xu J, Kepinski S, Bennett MJ, Zhang D (2018) Rice actin binding protein RMD controls crown root angle in response to external phosphate. Nat Commun 9:2346. https://doi.org/10.1038/s41467-018-04710-x
Jain M, Misra G, Patel RK, Priya P, Jhanwar S, Khan AW, Shah N, Singh VK, Garg R, Jeena G, Yadav M, Kant C, Sharma P, Yadav G, Bhatia S, Tyagi AK, Chattopadhyay D (2013) A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J 74:715–729. https://doi.org/10.1111/tpj.12173
Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:5–9. https://doi.org/10.1093/nar/gkn201
Jungk A (2001) Root hairs and the acquisition of plant nutrients from soil. J Plant Nutr Soil Sci 164:121–129
Kirik V, Simon M, Huelskamp M, Schiefelbein J (2004) The ENHANCER of TRY and CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev Biol 268:506–513. https://doi.org/10.1016/j.ydbio.2003.12.037
Kujur A, Bajaj D, Upadhyaya HD, Das S, Ranjan R, Shree T, Saxena MS, Badoni S, Kumar V, Tripathi S, Gowda CLL, Sharma S, Singh S, Tyagi AK, Parida SK (2015a) A genome-wide SNP scan accelerates trait-regulatory genomic loci identification in chickpea. Sci Rep 5:11166. https://doi.org/10.1038/srep11166
Kujur A, Bajaj D, Upadhyaya HD, Das S, Ranjan R, Shree T, Saxena MS, Badoni S, Kumar V, Tripathi S, Gowda CLL, Sharma S, Singh S, Tyagi AK, Parida SK (2015b) Employing genome-wide SNP discovery and genotyping strategy to extrapolate the natural allelic diversity and domestication patterns in chickpea. Front Plant Sci 6:162. https://doi.org/10.3389/fpls.2015.00162
Kujur A, Upadhyaya HD, Shree T, Bajaj D, Das S, Saxena MS, Badoni S, Kumar V, Tripathi S, Gowda CLL, Sharma S, Singh S, Tyagi AK, Parida SK (2015c) Ultra-high density intra-specific genetic linkage maps accelerate identification of functionally relevant molecular tags governing important agronomic traits in chickpea. Sci Rep 5:9468. https://doi.org/10.1038/srep09468
Leavitt RG (1904) Trichomes of the root in vascular cryptogams and angiosperms. Proc Boston Soc Nat Hist 31:273–313
Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: Genome association and prediction integrated tool. Bioinformatics 28:2397–2399. https://doi.org/10.1093/bioinformatics/bts444
Liu C, Zhang F, Zhang D et al (2018) Mycorrhiza stimulates root-hair growth and IAA synthesis and transport in trifoliate orange under drought stress. Sci Rep 8:1978. https://doi.org/10.1038/s41598-018-20456-4
Lynch JP, Brown KM (2001) Topsoil foraging - An architectural adaptation of plants to low phosphorus availability. Plant Soil 237:225–237. https://doi.org/10.1023/A:1013324727040
Macdonald GK, Bennett EM, Potter PA, Ramankutty N (2011) Agronomic phosphorus imbalances across the world ’ s croplands. Proc Natl Acad Sci 108:3086–3091. https://doi.org/10.1073/pnas.1010808108
Miguel MA (2004) Genotypic variation in root hairs and phosphorus efficiency in common bean (Phaseolus vulgaris L.). Doctoral desertation, Pennsylvania State University
Miguel MA, Postma JA, Lynch JP (2015) Phene synergism between root hair length and basal root growth angle for phosphorus Acquisition. Plant Physiol 167:1430–1439. https://doi.org/10.1104/pp.15.00145
Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun DJ, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci U S A 102:7760–7765. https://doi.org/10.1073/pnas.0500778102
Miura K, Lee J, Gong Q, Ma S, Jin JB, Yoo CY, Miura T, Sato A, Bohnert HJ, Hasegawa PM (2011) SIZ1 Regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiol 155:1000–1012. https://doi.org/10.1104/pp.110.165191
Muller M, Schmidt W (2004) Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiol 134:409–419. https://doi.org/10.1104/pp.103.029066
Nestler J, Wissuwa M, Bell RW (2016) Superior root hair formation confers root efficiency in some , but not all , rice genotypes upon P deficiency. Front Plant Sci 7:1935. https://doi.org/10.3389/fpls.2016.01935
Pandey BK, Mehra P, Verma L, Bhadouria J, Giri J (2017) OsHAD1 , a Haloacid Dehalogenase-Like APase , enhances phosphate accumulation. Plant Physiol 174:2316–2332. https://doi.org/10.1104/pp.17.00571
Pang J, Bansal R, Zhao H, Bohuon E, Lambers H, Ryan MH, Ranathunge K, Siddique KHM (2018a) The carboxylate-releasing phosphorus-mobilizing strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytol 219:518–529. https://doi.org/10.1111/nph.15200
Pang J, Zhao H, Bansal R, Bohuon E, Lambers H, Ryan MH, Siddique KHM (2018b) Leaf transpiration plays a role in phosphorus acquisition among a large set of chickpea genotypes. Plant Cell Environ 41:2069–2079. https://doi.org/10.1111/pce.13139
Pei W, Du F, Zhang Y et al (2012) Control of the actin cytoskeleton in root hair development. Plant Sci 187:10–18. https://doi.org/10.1016/j.plantsci.2012.01.008
Pires ND, Yi K, Breuninger H, Catarino B, Menand B, Dolan L (2013) Recruitment and remodeling of an ancient gene regulatory network during land plant evolution. Proc Natl Acad Sci U S A 110:9571–9576. https://doi.org/10.1073/pnas.1305457110
Pothuluri JV, Kissel DE, Whitney DA, Thien SJ (1986) Phosphorus uptake from soil layers having different soil test phosphorus levels. Agron J 78:991–994. https://doi.org/10.2134/agronj1986.00021962007800060012x
Ringli C, Baumberger N, Diet A, Frey B, Keller B (2002) ACTIN2 is essential for bulge site selection and tip growth during root hair development of Arabidopsis. Plant Physiol 129:1464–1472. https://doi.org/10.1104/pp.005777.1464
Salazar-Henao JE, Vélez-Bermúdez IC, Schmidt W (2016) The regulation and plasticity of root hair patterning and morphogenesis. Development 143:1848–1858. https://doi.org/10.1242/dev.132845
Sandhu N, Subedi SR, Singh VK, Sinha P, Kumar S, Singh SP, Ghimire SK, Pandey M, Yadaw RB, Varshney RK, Kumar A (2019a) Deciphering the genetic basis of root morphology , nutrient uptake , yield , and yield-related traits in rice under dry direct-seeded cultivation systems. Sci Rep 9:9334. https://doi.org/10.1038/s41598-019-45770-3
Sandhu N, Yadaw RB, Chaudhary B, Prasai H, Iftekharuddaula K, Venkateshwarlu C, Annamalai A, Xangsayasane P, Battan KR, Ram M, Cruz MTS, Pablico P, Maturan PC, Raman KA, Catolos M, Kumar A (2019b) Evaluating the performance of rice genotypes for improving yield and adaptability under direct seeded aerobic cultivation conditions. Front Plant Sci 10:159. https://doi.org/10.3389/fpls.2019.00159
Scheiner SM, Lyman RF (1989) The genetics of phenotypic plasticity I. Heritability. J Evol Biol 2:95–107. https://doi.org/10.1046/j.1420-9101.1989.2020095.x
Song L, Yu H, Dong J, Che X, Jiao Y, Liu D (2016) The molecular mechanism of ethylene-mediated root hair development induced by phosphate starvation. PLoS Genet 12:e1006194. https://doi.org/10.1371/journal.pgen.1006194
Stetter MG, Schmid K, Ludewig U (2015) Uncovering genes and ploidy involved in the high diversity in root hair density, length and response to local scarce phosphate in Arabidopsis thaliana. PLoS One 10:e0120604. https://doi.org/10.1371/journal.pone.0120604
Subedi SR, Sandhu N, Singh VK, Sinha P, Kumar S, Singh SP, Ghimire SK, Pandey M, Yadaw RB, Varshney RK, Kumar A (2019) Genome-wide association study reveals significant genomic regions for improving yield, adaptability of rice under dry direct seeded cultivation condition. BMC Genomics 20:471. https://doi.org/10.1186/s12864-019-5840-9
Takahashi M, Umetsu K, Oono Y, Higaki T, Blancaflor EB, Rahman A (2017) Small acidic protein 1 and SCFTIR1 ubiquitin proteasome pathway act in concert to induce 2,4-dichlorophenoxyacetic acid-mediated alteration of actin in Arabidopsis roots. Plant J 89:940–956. https://doi.org/10.1111/tpj.13433
Ühlken C, Horvath B, Stadler R, Sauer N, Weingartner M (2014) MAIN-LIKE1 is a crucial factor for correct cell division and differentiation in Arabidopsis thaliana. Plant J 78:107–120. https://doi.org/10.1111/tpj.12455
Upadhyaya HD, Dwivedi SL, Baum M et al (2008) Genetic structure, diversity, and allelic richness in composite collection and reference set in chickpea (Cicer arietinum L.). BMC Plant Biol 8:106. https://doi.org/10.1186/1471-2229-8-106
Varshney RK, Song C, Saxena RK et al (2013) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol 31:240–246. https://doi.org/10.1038/nbt.2491
Varshney RK, Thudi M, Roorkiwal M, He W, Upadhyaya HD, Yang W, Bajaj P, Cubry P, Rathore A, Jian J, Doddamani D, Khan AW, Garg V, Chitikineni A, Xu D, Gaur PM, Singh NP, Chaturvedi SK, Nadigatla GVPR, Krishnamurthy L, Dixit GP, Fikre A, Kimurto PK, Sreeman SM, Bharadwaj C, Tripathi S, Wang J, Lee SH, Edwards D, Polavarapu KKB, Penmetsa RV, Crossa J, Nguyen HT, Siddique KHM, Colmer TD, Sutton T, von Wettberg E, Vigouroux Y, Xu X, Liu X (2019) Resequencing of 429 chickpea accessions from 45 countries provides insights into genome diversity, domestication and agronomic traits. Nat Genet 51:857–864. https://doi.org/10.1038/s41588-019-0401-3
Vijayakumar P, Datta S, Dolan L (2016) ROOT HAIR DEFECTIVE SIX-LIKE4 (RSL4) promotes root hair elongation by transcriptionally regulating the expression of genes required for cell growth. New Phytol 212:944–953. https://doi.org/10.1111/nph.14095
Wickham H (2016) ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York
Williamson LC, Ribrioux SPCP, Fitter AH, Ottoline Leyser HM (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882. https://doi.org/10.1104/pp.126.2.875
Yan X, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265:17–29. https://doi.org/10.1007/s11104-005-0693-1
Yano K, Shibata S, Chen WL, Sato S, Kaneko T, Jurkiewicz A, Sandal N, Banba M, Imaizumi-Anraku H, Kojima T, Ohtomo R, Szczyglowski K, Stougaard J, Tabata S, Hayashi M, Kouchi H, Umehara Y (2009) CERBERUS, a novel U-box protein containing WD-40 repeats, is required for formation of the infection thread and nodule development in the legume-Rhizobium symbiosis. Plant J 60:168–180. https://doi.org/10.1111/j.1365-313X.2009.03943.x
Yi K, Menand B, Bell E, Dolan L (2010) A basic helix-loop-helix transcription factor controls cell growth and size in root hairs. Nat Genet 42:264–267. https://doi.org/10.1038/ng.529
Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–360. https://doi.org/10.1038/ng.546
Zhang C, Simpson RJ, Kim CM, Warthmann N, Delhaize E, Dolan L, Byrne ME, Wu Y, Ryan PR (2018) Do longer root hairs improve phosphorus uptake? Testing the hypothesis with transgenic Brachypodium distachyon lines overexpressing endogenous RSL genes. New Phytol 217:1654–1666. https://doi.org/10.1111/nph.14980
Zhu J, Kaeppler SM, Lynch JP (2005) Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant Soil 270:299–310. https://doi.org/10.1007/s11104-004-1697-y
Zhu J, Zhang C, Lynch JP (2010) The utility of phenotypic plasticity of root hair length for phosphorus acquisition. Funct Plant Biol 37:313–322
Zygalakis KC, Kirk GJD, Jones DL, Wissuwa M, Roose T (2011) A dual porosity model of nutrient uptake by root hairs. New Phytol 192:676–688. https://doi.org/10.1111/j.1469-8137.2011.03840.x
Funding
This work was supported by the DBT-Innovative Young Biotechnologist Award (IYBA) [BT/010/IYBA/2016/04]. PSK acknowledges DBT-Junior Research Fellowship (JRF).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Supplementary Figure S1
Phenotyping pipeline and root hair measurement for chickpea accessions in +P and in –P condition. (PNG 5.23 mb)
Supplementary Figure S2
Percentage change in root hair length from +P to –P condition in 100 desi chickpea accessions. (Green bars- Increase, Red bars- Decrease). (PNG 5.23 mb)
Supplementary Figure S3
Representative image of chickpea accession Vaibhav in +P and –P condition. (PNG 5.23 MB)
Supplementary Figure S4
Genome-wide association study for the root hair length trait in different conditions using CMLM model. (PNG 5.23 mb)
ESM 1
(DOCX 26 kb).
Rights and permissions
About this article
Cite this article
Kohli, P.S., Kumar Verma, P., Verma, R. et al. Genome-wide association study for phosphate deficiency responsive root hair elongation in chickpea. Funct Integr Genomics 20, 775–786 (2020). https://doi.org/10.1007/s10142-020-00749-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-020-00749-6